Rotational head acceleration and traumatic brain injury in combat sports: a systematic review

Abstract Background Traumatic brain injury (TBI) in combat sports is relatively common, and rotational acceleration (RA) is a strong biomechanical predictor of TBI. This review summarizes RA values generated from head impacts in combat sport and puts them in the context of present evidence regarding TBI thresholds. Sources of data PubMed, EMBASE, Web of Science, Cochrane Library and Scopus were searched from inception to 31st December 2021. Twenty-two studies presenting RA data from head impacts across boxing, taekwondo, judo, wrestling and MMA were included. The AXIS tool was used to assess the quality of studies. Areas of agreement RA was greater following direct head strikes compared to being thrown or taken down. RA from throws and takedowns was mostly below reported injury thresholds. Injury thresholds must not be used in the absence of clinical assessment when TBI is suspected. Athletes displaying signs or symptoms of TBI must be removed from play and medically evaluated immediately. Areas of controversy Methodological heterogeneity made it difficult to develop sport-specific conclusions. The role of headgear in certain striking sports remains contentious. Growing points RA can be used to suggest and assess the effect of safety changes in combat sports. Gradual loading of training activities based on RA may be considered when planning sessions. Governing bodies must continue to work to minimize RA generated from head impacts. Areas timely for developing research Prospective research collecting real-time RA data is required to further understanding of TBI in combat sports.


Introduction
Traumatic brain injury (TBI) occurs when external forces transmitted to the head cause neuropathologic damage and/or dysfunction. 1 Examples of TBI include concussion, diffuse axonal injury (DAI) and acute subdural haematoma (ASDH). TBI is classified as mild, moderate or severe. Clinical signs vary and include new-onset loss of consciousness (LOC), posttraumatic amnesia (PTA), alterations in mental state (e.g. confusion) and focal neurological deficit. 2 Most athletes recover fully within one week of TBI, yet there is growing evidence of long-term neurological sequelae including recurrent headache, cognitive impairment and death. 1 TBI is common in combat sports, with approximately 300 000 cases diagnosed every year. 3 Combat sports are generally of a striking (boxing, taekwondo) or grappling (judo, wrestling) nature, with mixed martial arts (MMA) combining multiple disciplines into one sport that includes both striking and grappling. TBI can therefore occur following direct head strikes or after being thrown or taken down. The rapid acceleration-deceleration forces generated upon impact cause vigorous movements of the brain within the skull, resulting in widespread neuronal and vascular damage in proportion to the degree of acceleration experienced. 4 Acceleration can be linear or rotational, depending on head movement relative to the body. Although both types can be present during an impact, rotational acceleration (RA) is more strongly implicated in TBI. 5 Brain tissue tends to deform following the application of shearing forces, and approximately 90% of the total shearing stresses produced can be attributed to RA. 6 TBI is likely underdiagnosed for several reasons, including the absence of a mandatory injuryreporting system and the lack of more typical signs at presentation. 7 The confusion surrounding its diagnosis has led to inconsistent management, with athletes returning inappropriately early to sport, thus increasing the risk of further TBI. 7,8 Various RA thresholds have been suggested for injuries such as concussion (4500 rad/s 2 ), DAI and ASDH (10 000 rad/s 2 ). 4,9,10 We systematically reviewed the available data on RA generated from combat sport impacts to the head and put these in the context of proposed TBI thresholds.

Methods
The search strategy and reporting of this review was conducted in accordance with the Preferred The full text of the relevant articles was retrieved for further assessment, and studies that met the eligibility criteria were included. Any disagreements regarding the eligibility of a study were resolved by consensus and involved the opinion of a third researcher.

Data extraction and analysis
Data extracted from eligible studies included author, year, country, study design, sport investigated, data collection method, technique/location of impact and peak/average peak (±SD) RA. Additional details or comparators were recorded if present. Head impact locations were grouped into 'front' (and forehead), 'side', 'top', 'back' and 'jaw' in line with research in this field. 11 The higher value of studies reporting multiple impacts to the same location (i.e. left and right 'side') was always taken. One reviewer (KSL) extracted the data and a second reviewer (NM) independently verified the data. Meta-analysis was not possible given the heterogeneity between studies. OR 'combat sport * ' OR 'mixed martial arts' OR MMA) AND (rotation * OR angular OR accel * OR biomechanic * OR kinematic * OR movement * OR impact * OR device * OR punch * OR kick * OR strike * OR throw * OR takedown * OR technique * ) AND (head OR 'head impact * ' OR brain OR injur * OR traum * OR 'traumatic brain injur * ' OR TBI OR concussion) A descriptive analysis of the data was performed with reference to the proposed TBI thresholds.

Quality assessment
The same two reviewers independently assessed the methodological quality of each investigation using the Appraisal tool for Cross-Sectional Studies (AXIS). 12 The AXIS tool consists of 20 items and serves as a means of critical appraisal by addressing study designs, reporting quality and risk of bias. 12 Four items (3,7,13,14) were removed from scoring across all studies as it was not appropriate to assess non-response. 12 Further three items (5,6,20) were removed from studies involving nonhuman participants. 12,13 Scores were reported as percentages to account for the changes made to the scoring system. Studies were given one point for items met and none for items not met (or where this was unclear). Interpretation of overall study quality was left at the discretion of the research team. Disagreements between authors were resolved by consensus and no study was excluded based on quality assessment.

Study selection
The initial literature search identified 8065 studies, and 5491 remained following duplicate removal. Additional two studies were identified during background searches. Title and abstract screening excluded 5422 studies and left 69 for full-text screening. Of these, 22 studies met the inclusion criteria. The most common reason for exclusion was RA not being measured (n = 35). No further studies were identified from screening the reference lists of relevant reviews identified during the literature search. A full breakdown of the selection process can be seen in Figure 1.

Wrestling
One HH study 17

Discussion
This review summarizes RA data from combat sport head impacts. RA was greater following direct strikes to the head compared to being thrown or taken down. Several impacts exceeded the proposed concussion threshold (4500 rad/s 2 ) in boxing, taekwondo and MMA, with some also exceeding the proposed DAI and ASDH threshold (10 000 rad/s 2 ). RA from impacts in judo and wrestling was almost always below injury thresholds. This suggests that athletes in boxing, taekwondo and MMA are at greater risk of TBI.

Headgear
Headgear featured more often in striking sports (boxing, taekwondo). The physical designs used had been sanctioned by the appropriate governing bodies. Our findings show that head impacts in these sports can produce dangerously high RA values. Nevertheless, the use of headgear remains contentious. Two studies (both MD) compared RA from different boxing impacts with and without headgear: every impact (hook punch, front, side, jaw) without headgear was in excess of 4500 rad/s. 2 When used, RA was lowered to subthreshold levels for hook punches (1740 rad/s 2 ), front (4335 rad/s 2 ) and side impacts (4323 rad/s 2 ). RA, however, albeit reduced, remained above the concussion threshold for impacts to the jaw (7173 rad/s 2 ). Interestingly, a different HD study, which did not use headgear, measured RA from jaw impacts to be less (6896 rad/s 2 ) than that of the aforementioned value. 19 This might be explained by the jaw being poorly protected on certain designs, yet it would suggest that headgear does not always ensure safe RA values in boxing. In two other studies (both HD) using headgear, front impacts (6344-14 065 rad/s 2 ) exceeded 4500 and 10 000 rad/s. 2 Once more, if we compare this to another study (also HD), we see that RA measured with headgear (6344 rad/s 2 ) was greater than without (5452 rad/s 2 ).
Although the sample is small, the use of headgear appears to offer some benefit RA in boxing. However, it should be acknowledged that there is no clear and obvious pattern: the lowest RA in boxing was measured in a study that did not use headgear. Despite this published evidence, in 2013, the Amateur International Boxing Association (AIBA) banned headgear in all forms of competition, after a study identified that boxing without headgear lowered the chance of a fight ending in referee stoppage by 43%. 36 Headgear is believed to increase the target area for opponents and decrease peripheral vision of the wearing athlete, and misconceptions surrounding the protective potential of headgear can result in more aggressive fighting styles that carry a greater risk of being hit, but these claims have been disputed. 37 ,38 Impact measures such as RA do not appear to have been considered, and headgear (or equivalent) has also been shown to lower RA in sports such as American football and rugby union. 39,40 This suggests that further research is necessary in boxing to assess the effect of such protective equipment on RA. Moreover, a recent systematic review concluded that the current evidence did not support the decision to prohibit the use of headgear in the sport. 41 RA remained high in taekwondo despite athletes requiring headgear, and multiple impacts exceeded 10 000 rad/s 2 . Only one study recorded a subthreshold average RA (4455 rad/s 2 ) on impact, and this would suggest that taekwondo athletes are most at risk of possibly severe TBI. 29 For this reason, improvements to current headgear designs may be necessary to increase athlete safety. If changes to protective equipment were not to be sufficient, a revision of rules may be warranted. In judo, for example, throws carrying a high injury risk (kanibasami, kawazu-gake) are now forbidden, 42 Headgear is not commonly worn in grappling sports (judo, wrestling), nor in MMA. One study documented that MMA athletes used headgear exclusively during sparring, with recorded RA (1766 rad/s 2 ) much lower than when measured in competition (3773 rad/s 2 ). In judo, a stronger emphasis is placed on correct technique to reduce the risk of TBI, and similar RA values were obtained from throws irrespective of whether or not headgear was worn. Amateur wrestlers are required to wear headgear in some countries, but not in international senior competition. Even so, this is primarily for ear protection, and such headgear offers no recognized protection against TBI.

Associated injury/LOC
RA resulting in concussion was recorded in two MMA studies (both HH). In concussive impacts (7560.8-7561 rad/s 2 ), RA was greater than in those causing no injury (5055.7-7069.5 rad/s 2 ). A similar trend was observed in boxing, where RA from LOC punches (11279.5 rad/s 2 ) was significantly higher than non-LOC punches (6145.5 rad/s 2 ).
Non-injury-causing impacts, in striking sports particularly, easily exceed proposed thresholds, and this includes impacts that occur during lowerintensity and non-competitive (i.e. sparring) environments. One study found RA during MMA sparring to be above the concussion threshold (5055.7 rad/s 2 ). While sparring is not directly applicable to real fighting, RA can remain high and impacts are potentially injurious. There is a significant risk of TBI to athletes in competitive and non-competitive settings, who, critically, may not be visibly incapacitated. It is vital that those displaying signs or symptoms consistent with TBI are immediately removed from play and evaluated by a medical professional.

Ukemi (breakfall) and under-mats
Judo players are taught to perform ukemi (breakfall) when landing to minimize the risk of TBI. Correct ukemi technique prevents direct head contact with the mat and can therefore lower RA after being thrown. We see its value when comparing athlete and dummy studies, given that only athletes can execute ukemi. RA from osoto-gari in HH studies (679.4-693.2 rad/s 2 ) was lower than that in HD studies (3315-5081 rad/s 2 ), and this is also the case for ouchi-gari and seoi-nage throws. Judo players should continue to learn optimal technique before practising throws with a high risk of injury. Under-mats may help to prevent injury in judo, but the increased RA with their use in ouchi-gari raises questions about their overall efficacy.

Clinical implications and future work
The findings of the present systematic review should inform future research and highlight areas in combat sports where action can be taken. Although all studies were of a good quality, a small number of studies were less than optimal, and the heterogeneity of the available data made it challenging to formulate sport-specific recommendations. We acknowledge that differences between individual methodologies (HH, HD, MD), along with the specific testing conditions of each study, will have influenced the data produced by the various investigations. In a laboratory (HD, MD) setting, this includes athletes impacting dummies with various amounts of force, and mechanical devices impacting these devices at fixed velocities. Equally, there are physical variables in entirely human (HH) studies that cannot be replicated in the laboratory. Fatigue, in particular, negatively affects reaction times and consistency (increasing susceptibility to TBI) but reduces the magnitude of impacts delivered. 43,44 Altogether, this makes it difficult to apply laboratory data to physical combat situations, and comparing data across study types must be done with caution.
We acknowledge that some of the investigations included in the present study are laboratory based. Laboratory RA data demonstrate the capability of combat sport athletes to inflict catastrophic and lifethreatening damage in a practice, not competition, situation from one single impact. For this reason, it would be unethical to replicate such studies with human participants. Laboratory data do not mirror competitive fighting, but these results highlight impacts in these arguably lower-intensity situations can cause TBI: RA likely increases in higher-intensity environments.
The possible error associated with the delivery of mechanical impacts should also be discussed. The Hybrid III ATD headform, for instance, overestimates RA by 8%. 45 Moreover, these impacts were delivered linearly and do not represent the rotational body motion of athletes. Above all, the thresholds discussed in this review are only some of those that exist in literature: evidently, different thresholds would change the way in which our results are interpreted. RA thresholds should not be used in the absence of physical assessment to diagnose TBI. For example, osoto-gari is strongly associated with ASDH in judo, and a maximum RA of 5081.3 rad/s 2 is evidently below the proposed injury threshold. This may seem unsurprising, as we know composite variables to be more sensitive in predicting TBI. However, lower RA causes less structural brain damage; hence, RA can continue to offer direction for safety changes in combat sports. 46 Meanwhile, it is essential that governing bodies strive to minimize RA produced from head impacts, and we recommend that future prospective research involving combat sport athletes is performed to achieve this. We encourage the use of appropriate instrumented equipment to allow for the collection of in vivo RA data. 45,47 Head Impact Telemetry (HIT) is an example of a validated system used in sport and can be incorporated into headgear and mouthguards to collect information about RA. 45 Other systems have enabled the development of instrumented headbands, skullcaps and skin patches, but currently lack validation.
Ultimately, the diagnosis of TBI in combat sports is facilitated by the presence of on-site physicians. Athletes are monitored carefully in the professional setting, but most compete in environments where trained medical personnel are not routinely available, and assessment is left in the hands of athletes and coaches. Knowledge of TBI in these groups remains poor, and it is estimated that 40% of athletes immediately return to play after a suspected TBI. 48 There is a need for education programmes to be made available in combat sports and it is unfair to assume a degree of clinical competency from coaches or officials. RA can help to contextualize TBI in combat sports as the relevant techniques can be understood by athletes, coaches and researchers alike. Thus, RA can be used to assess the risk of training activities and ensure proper planning of training to offer adequate rest between sessions. Sessions should also follow gradual loading and start with lower RA activities before moving on to higher RA activities to reduce risk of TBI. This would arguably be of most benefit in MMA, given the differences in RA between strikes and throws. A recent study also found that periodization of training load was largely absent amongst MMA athletes. 49 RA, along with other measures of training intensity, may help to prioritize player safety, prevent overtraining and ensure that the enjoyment of combat sport is maintained. 50 Finally, the cumulative effect of subthreshold impacts in combat sports should not be forgotten. Growing evidence links the effects of repeated head impacts to dementia, depression and chronic traumatic encephalopathy (CTE). 51 There is also a greater possibility of musculoskeletal injury following TBI in sport, and neuromuscular risk factors should be considered when determining return to play. 52 The mismanagement of these impacts increases the short-term risk of severe TBI. 53

Limitations
There are certainly some limitations to the present systematic review. Firstly, we collated RA from studies presenting peak, and average peak, values. In those measuring average peak (±SD) RA, the entire range was not consistently available; thus, we are not able to comment on this any further. Secondly, we did not consider the effect of any other biomechanical variables (i.e. impact velocity, impulse time), albeit beyond the scope of the present work. Lastly, the characteristics of athletes in studies involving human participants (age, sex, height, weight, experience level) were not presented in the original studies. This is also likely to influence our data.

Conclusion
Head impacts in combat sports produce significant RA, and various thresholds for different types of TBI have been proposed. Direct head impacts in striking sports produced greater RA values than impacts from throws or takedowns in grappling sports and appear to put athletes at greater risk of TBI. Differences in study methodologies and testing conditions meant that accurate sport-specific conclusions could not be drawn. However, the present systematic review serves as a reminder that dangerously high RA values can be generated even in non-competitive environments (laboratory, sparring). The use of headgear in boxing lowered RA, allowing RA to reach subthreshold levels. Similarly, modifications to headgear design in taekwondo may be necessary given the substantial RA generated from rotating kicks. RA remains a useful predictor of TBI, as lower values are associated with less structural brain damage. Non-injury-causing impacts can exceed TBI thresholds and therefore carry a real risk of injury, and it is imperative that athletes showing signs or symptoms consistent with TBI are removed from play and medically assessed. Greater awareness of RA in combat sports affords coaches the opportunity to risk stratify training activities and ensure appropriate rest periods between sessions. Suitable educational tools must also be made available to athletes and coaches of all abilities. Future prospective research should measure RA from real-life impacts and document associated injury outcomes in order to further our understanding of TBI in combat sports. For the time being, sporting governance must strive to minimize RA from head impacts to maximize athlete safety.